Male sex pheromones and the phylogeographic structure of the Lutzomyia longipalpis species complex (Diptera: Psychodidae) from Brazil and Venezuela

American Journal of Tropical Medicine and Hygiene

Volumn 73, Issue 4, 2005, Pages 734-743

  Watts, Phillip C ^b   Hamilton, J Gordon C ^a   Ward, Richard D ^a   Noyes, Harry A ^b   Souza, Nataly A ^c   Kemp, Stephen J ^b   Feliciangeli, M Dora ^d   Brazil, Reginaldo ^e   Maingon, Rhayza D C ^a  

^a KEELE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

^d UNIVERSIDAD DE CARABOBO   (Venezuela)

^e Laboratorio de Bioquimica e Fisiologia de Insetos   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

9 METHYLGERMACRENE B; GERMACRANOLIDE DERIVATIVE; METHYL GROUP; SEX PHEROMONE; UNCLASSIFIED DRUG;

ARTICLE; BRAZIL; CLUSTER ANALYSIS; DISEASE CARRIER; FLY; GENE LOCUS; GENETIC VARIABILITY; LEISHMANIA CHAGASI; LEISHMANIA INFANTUM; LUTZOMYIA CRUZI; LUTZOMYIA LONGIPALPIS; LUTZOMYIA PSEUDOLONGIPALPIS; MICROSATELLITE MARKER; NONHUMAN; PHYLOGEOGRAPHY; POPULATION; PSYCHODIDAE; VENEZUELA;

DIPTERA; LEISHMANIA DONOVANI CHAGASI; LEISHMANIA INFANTUM; LUTZOMYIA CRUZI; LUTZOMYIA LONGIPALPIS; LUTZOMYIA PSEUDOLONGIPALPIS; PSYCHODIDAE;

EID: 26844468528     PISSN: 00029637     EISSN: None     Source Type: Journal    
DOI: 10.4269/ajtmh.2005.73.734     Document Type: Article

References (70)

1. Young DG, Duncan MA, 1994. Guide to the Identification and Geographic Distribution of Lutzomyia Sand Flies in Mexico, West Indies, Central and South America (Diptera: Psychodidae). Gainesville, FL: American Entomologic Institute.
2. Mauricio IL, Howard MK, Stothard JR, Miles MA, 1999. Genomic diversity in the Leishmania donovani complex. Parasitology 119: 237-246.
3. Ashford RW, Desjeux P, de Raadt P, 1992. Estimation of population at risk of infection and number of cases of leishmaniasis. Parasitol Today 8: 104-105.
4. Arias JR, Monteiro PS, Zicker F, 1996. The re-emergence of visceral leishmaniasis in Brazil. Emerg Infect Dis 2: 145-146.
5. Author unknown, 2003. Brazil: Health Situation Analysis and Trends Summary. Accessed April 5, 2004. Available from http://www.paho.org
6. Franke CR, Ziller M, Staubach C, Latif M, 2002. Impact of the E1 Nino/southern oscillation on visceral leishmaniasis, Brazil. Emerg Infect Dis 8: 914-917.
7. Guerra JAO, Barros MLB, Ferreira Fe N, Guerra MVF, Castellon E, Gomes Paes M, Sherlock IA, 2004. Leishmaniose visceral entre indios no Estado de Roraima, Brasil. Aspectos clinicoepidemiológicos de casos observados no periodo de 1989 a 1993. Rev Soc Bras Med Trop 37: 305-311.
8. Marzochi MC de A, Marzochi KBF, 1994. Tegumentary and visceral leishmaniasis in Brazil - Emerging anthropozoonosis and possibilities for their control. Cad Saude Publica 10: 359-375.
9. Alves Gama ME, Lopes Costa JM, Castro Gomes CM, Pereira Corbett CE, 2004. Subclinical form of American visceral leishmaniasis. Mem Inst Oswaldo Cruz 99: 889-893.
10. Uribe S, 1999. The status of the Lutzomyia longipalpis species complex and possible implications for Leishmania transmission. Mem Inst Oswaldo Cruz 94: 729-734.
11. Warburg A, Saraiva E, Lanzaro GC, Titus RG, Neva F, 1994. Saliva of Lutzomyia longipalpis sibling species differs in its composition and capacity to enhance leishmaniasis. Philos Trans R Soc Lond B Biol Sci 345: 223-230.
12. Lanzaro GC, Warburg A, 1995. Genetic variability in phlebotomine sandflies: possible implications for leishmaniasis epidemiology. Parasitol Today 11: 151-154.
13. Noyes HA, Chance M, Ponce C, Ponce E, Maingon RDC, 1997. Leishmania chagasi: genotypically similar parasites from Honduras cause both visceral and cutaneous leishmaniasis in humans. Exp Parasitol 85: 264-273.
14. Yin H, Norris DE, Lanzaro GC, 2000. Sibling species in the Lutzomyia longipalpis complex differ in levels of mRNA expression for the salivary peptide, maxadilan. Insect Mol Biol 9: 309-314.
15. Arrivillaga JC, Feliciangeli MD, 2001. Lutzomyia pseudolongipalpis: The first new species within the longipalpis (Diptera-Psychodidae: Phlebotominae) complex from La Rinconada, Curarigua, Lara State, Venezuela. J Med Entomol 38:783-790.
16. Mangabeira O, 1969. Sobre a sistematica e biologia dos Phlebotomus do Ceará. Rev Bras Malariol Doenças Trop 12: 3-26.
17. Lane RP, Ward RD, 1984. The morphology and possible function of abdominal patches in males of two forms of the leishmaniasis vector Lutzomyia longipalpis (Diptera: Phlebotominae). Cah ORSTOM Ser Entomol Med Parasitol 22: 245-249.
18. Ward RD, Ribeiro A, Ready PD, Murtagh A, 1983. Reproductive isolation between different forms of Lutzomyia longipalpis (Lutz & Neiva) (Diptera:Psychodidae) the vector of Leishmania donovani chagasi Cunha & Chagas and its significance to Kala-azar distribution in South America. Mem Inst Oswaldo Cruz 78: 269-280.
19. Ward RD, Phillips A, Burnet B, Marcondes CB, 1988. The Lutzomyia longipalpis complex: reproduction and distribution. Service MW, ed. Biosystematics of Haematophagous Insects. Oxford, United Kingdom: Oxford University Press, 258-269.
20. Hamilton JGC, Dawson GW, Pickett JA, 1996a. 9-Methyl-germacrene B, a novel homosequiterpene from sex pheromone glands of Lutzomyia longipalpis (Diptera: Psychodidae) from Lapinha, Brazil. J Chem Ecol 22:1477-1491.
21. Hamilton JGC, Dawson GW, Pickett JA, 1996b. 3-Methyl-α-himachalene; sex pheromone of Lutzomyia longipalpis (Diptera:Psychodidae) from Jacobina, Brazil. J Chem Ecol 22: 2331-2340.
22. Hamilton JGC, Hooper AM, Ibbotson HC, Kurosawa S, Mori K, Muto S, Pickett JA, 1999(a). 9-Methylgermacrene-B is confirmed as the sex pheromone of the sandfly Lutzomyia longipalpis from Lapinha, Brazil, and the absolute stereochemistry is defined as S. Chem Comm 2335-2336.
23. Hamilton JGC, Hooper AM, Mori K, Pickett JA, Sano S, 1999(b). 3-Methyl-α-himachalene is confirmed, and the relative stereochemistry defined, by synthesis as the sex pheromone of the sandfly Lutzomyia longipalpis from Jacobina, Brazil. Chem Comm 355-356.
24. Hamilton JGC, Brazil RP, Maingon RDC, 2004. A fourth chemotype of Lutzomyia longipalpis (Diptera: Psychodidae) from Jaíbas, Minas Gerais State, Brazil. J Med Entomol 41: 1021-1026.
25. Souza NA, Ward RD, Hamilton JGC, Kyriacou CP, Peixoto AA, 2002. Copulation songs in three siblings of Lutzomyia longipalpis (Diptera: Psychodidae). Trans R Soc Trop Med Hyg 96: 102-103.
26. Souza NA, Vigoder FM, Araki AS, Ward RD, Kyriacou CP, Peixoto AA, 2004. Analysis of the copulation songs of Lutzomyia longipalpis in six populations from Brazil. J Med Entomol 41: 906-913.
27. Coyne JA, Orr HA, 2004. Studying speciation. Coyne JA, Orr HA. Eds. Speciation. Sunderland, MA: Sinauer Associates Inc., 65-82.
28. Bauzer LGSR, Souza NA, Ward RD, Kyriacou C, Peixoto AA, 2002a. The period gene and genetic differentiation between three Brazilian populations of L. longipalpis. Insect Mol Biol 11: 315-323.
29. Bauzer LGSR, Gesto JSM, Souza NA, Ward RD, Hamilton JGC, Kyriacou C, Peixoto AA, 2002b. Molecular divergence in the period gene between two putative sympatric species of the Lutzomyia longipalpis complex. Mol Biol Evol 19:1624-1627.
30. Lanzaro GC, Ostrovska K, Herrero MV, Lawyer PG, Warburg A, 1993. Lutzomyia longipalpis is a species complex: genetic divergence and interspecific hybrid sterility among three populations. Am J Trop Med Hyg 48: 839-847.
31. Mutebi JP, Rowton E, Herrero MV, Ponce C, Belli A, Valle S, Lanzaro GC, 1998. Genetic variability among populations of the sand fly Lutzomyia longipalpis (Diptera: Psychodidae) from Central America. J Med Entomol 35: 169-174.
32. Yin H, Mutebi JP, Marriott S, Lanzaro GC, 1999. Metaphase karyotypes and G-banding in sandflies of the Lutzomyia longipalpis complex. Med Vet Entomol 13: 72-77.
33. Lampo M, Torgerson D, Márquez LM, Rinaldi M, García CZ, Arab A, 1999. Occurrence of sibling species of Lutzomyia longipalpis (Diptera:Psychodidae) in Venezuela: first evidence from reproductively isolated sympatric populations. Am J Trop Med Hyg 61: 1004-1009.
34. Arrivillaga JC, Rangel YN, Oviedo M, Feliciangeli MD, 2000. Correlated morphologic and genetic diversity among Lutzomyia longipalpis (Diptera: Psychodidae) collections in Venezuela. J Am Mosq Control Assoc 16: 171-174.
35. Mukhopadhyay J, Ghosh K, Azevedo CR, Rangel EF, Munstermann LE, 1998. Genetic polymorphism of morphological and biochemical characters in a Natal, Brazil, population of Lutzomyia longipalpis (Diptera:Psychodidae). J Am Mosq Control Assoc 14: 277-282.
36. Mutebi JP, Alexander B, Sherlock I, Wellington J, Souza AA, Shaw J, Rangel EF, Lanzaro GC, 1999. Breeding structure of the sandfly Lutzomyia longipalpis (Lutz & Neiva) in Brazil. Am J Trop Med Hyg 61: 149-157.
37. Azevedo ACR, Monteiro FA, Cabello PH, Souza NA, Rosa-Freitas MG, Rangel EF, 2000. Studies on populations of Lutzomyia longipalpis (Lutz & Neiva, 1912) (Diptera: Psychodidae: Phlebotominae) in Brazil. Mem Inst Oswaldo Cruz 95: 305-322.
38. Arrivillaga JC, Norris DE, Feliciangeli MD, Lanzaro GC, 2002. Phylogeography of the neotropical sand fly Lutzomyia longipalpis inferred from mitochondrial DNA sequences. Infect Genet Evol 2: 83-95.
39. Arrivillaga J, Mutebi JP, Pinango H, Norris D, Alexander B, Feliciangeli MD, Lanzaro GC, 2003. The taxonomic status of genetically divergent populations of Lutzomyia longipalpis (Diptera: Psychodidae) based on the distribution of mitochondrial and isozyme variation. J Med Entomol 40: 615-627.
40. Hodgkinson VH, Birungi J, Quintana M, Deitze R, Munstermann LE, 2003. Mitochondrial cytochrome b variation in populations of the visceral leishmaniasis vector Lutzomyia longipalpis across eastern Brazil. Am J Trop Med Hyg 69: 386-392.
41. Lins RMMA, Oliveira SG, Souza NA, de Queiroz RG, Justiniano SCB, Ward RD, Kyriacou CP, Peixoto AA, 2002. Molecular evolution of the cacophony IVS6 region in sandflies. Insect Mol Biol 11: 117-122.
42. Maingon RDC, Ward RD, Hamilton JGC, Noyes HA, Souza N, Kemp SJ, Watts PC, 2003. Genetic differentiation of two sibling species of Lutzomyia longipalpis (Diptera: Psychodidae) that produce distinct male sex pheromones in Sobral, Ceara State, Brazil. Mol Ecol 12: 1879-1894.
43. Bottechia M, Oliveira SG, Bauzer LGSR, Souza NA, Ward RD, Garner KJ, Kyriacou CP, Peixoto AA, 2004. Genetic divergence in the cacophony IVS6 intron among five Brazilian populations of Lutzomyia longipalpis. J Mol Evol 58:754-761.
44. Krzywinski J, Besansky NJ, 2003. Molecular systematics of Anopheles: from subgenera to subpopulations. Annu Rev Entomol 48: 111-139.
45. Modi GB, Tesh RB, 1983. A simple technique for mass rearing Lutzomyia longipalpis and Phlebotomus papatasi (Diptera: Psychodidae). J Med Entomol 20: 568-569.
46. Collins FH, Mendez MA, Rasmussen MO, Mehaffey PC, Besansky NJ, Finnerty V, 1987. A ribosomal RNA gene probe differentiates member species of the Anopheles gambiae complex. Am J Trop Med Hyg 37: 37-41.
47. Watts PC, Boyland E, Noyes HA, Maingon RDC, Kemp SJ, 2001. Polymorphic dinucleotide microsatellite loci in the sandfly Lutzomyia longipalpis (Diptera: Phlebotominae). Mol Ecol Notes 2: 60-61.
48. Raymond M, Rousset F, 1995. GENEPOP, Version 1.2. Population genetics software for exact tests and ecumenicism. J Hered 86: 248-249.
49. Schneider S, Roessli D, Exoffier C, 2000. ARLEQUIN Version 2000. Genetics and Biometry. Geneva, Switzerland: University of Geneva.
50. Wright S, 1951. The genetical structure of populations. Ann Eugen 15: 323-354.
51. Langella O, 2002. POPULATIONS 1.2.28. Population Genetic Software (Individuals or Populations Distances, Phylogenetic Trees). Available from http://www.cnrs-gif.fr/pge/bioinfo/populations/index.php
52. Gaggiotti OE, Lange O, Rassmann K, Gliddon C, 1999. A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol Ecol 8:1513-1520.
53. Weir BS, Cockerham CC, 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
54. Roussel F, 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145: 219-228.
55. Saitou N, Nei M, 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
56. Rice WR, 1989. Analyzing tables of statistical tests. Evolution 43: 223-225.
57. Sunnucks P, 2000. Efficient genetic markers for population biology. Trends Ecol Evol 15: 199-203.
58. Ellegren H, Moore S, Robinson N, Byrne K, Ward W, Sheldon BC, 1997. Microsatellite evolution - a reciprocal study of repeat lengths at homologous loci in cattle and sheep. Mol Biol Evol 14: 854-860.
59. Mukhopadhyay J, Rangel EF, Ghosh K, Munstermann LE, 1997. Patterns of genetic variability in colonized strains of Lutzomyia longlpalpis (Diptera:Psychodidae) and its consequences. Am J Trop Med Hyg 57: 216-221.
60. Lanzaro GC, Alexander B, Mutebi JP, Montoya-Lerma J, Warburg A, 1998. Genetic variation among natural and laboratory colony populations of Lutzomyia longipalpis (Lutz & Nieva, 1912) (Diptera: Psychodidae) from Colombia. Mem Inst Oswaldo Cruz 93: 65-69.
61. Uribe-Soto SI, Lehmann T, Rowton ED, Velez ID, Porter CH, 2001. Speciation and population structure in the morphospecies Lutiomyia longipalpis (Lutz & Neiva) as derived from the mitochondrial ND4 gene. Mol Phylogenet Evol 10: 84-93.
62. Hamilton JGC, Maingon RDC, Alexander B, Ward RD, Brazil RP, 2005. Analysis of the sex pheromone extract of individual male Lutzomyia longipalpis from six regions in Brazil. Med Vet Entomol 19: (in press).
63. Hamilton JGC, Brazil RP, Campbell-Lendrum D, Davies CR, Kelly DW, Pessoa FAC, de Queiroz RG, 2002. Distribution of putative male sex pheromones among Lutzomyia sandflies (Diptera: Psychodidae). Ann Trop Med Parasitol 96: 83-92.
64. Mares MA, Genoways HH, 1981. South American Landscapes and their mammals. The Pymatuning Symposia in Ecology, Special Publication Series. Volume 6. Pittsburgh: University of Pittsburgh Press, 53-75.
65. Huber O, 1987. Neotropical savannas: their flora and vegetation. Trends Ecol Evol 2: 67-71.
66. Haffer J, 1969. Speciation in Amazonian forest birds. Science 165: 131-137.
67. Hamilton JGC, Ward RD, Dougherty MJ, Maingon R, Ponce C, Ponce E, Noyes H, Zeledon R, 1996. Comparison of the sex-pheromone components of Lutzomyia longipalpis (Diptera: Psychodidae) from areas of visceral and atypical cutaneous leishmaniasis in Honduras and Costa Rica. Ann Trop Med Parasitol 90: 533-541.
68. dos Santos S, Arias JR, Hoffmann MP, Grotta Furlan MB, Wilson FF, Pereira C, Ferreira L, 2003. The presence of Lutzomyia longipalpis in a focus on American visceral leishmaniasis where the only proven vector is Lutzomyia cruzi, Corumbá, Mato Grosso do Sul State. Rev Soc Bras Med Trop 36: 633-634.
69. Brazil RP, Hamilton JGC, 2002. Isolation and identification of 9-methylgermacrene-B as the putative sex pheromone of Lutzomyia cruzi (Mangabeira, 1938) (Diptera: Psychodidae). Mem Inst Oswaldo Cruz 97: 435-436.
70. Greenberg AJ, Moran JR, Coyne JA, Wu CI, 2003. Ecological adaptation during incipient speciation revealed by precise gene replacement. Science 302: 1754-1757.